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Influenza A virus in swine: situation in European countries

In the wake of the so-called “swine flu” a European surveillance program was carried out in 2013-2015: H1N1pdm is present in several European countries, and at particularly high prevalence in Britain and Ireland.

Monday 19 December 2016 (1 years 3 months 5 days ago)

Influenza A virus (IAV) infections cause significant morbidity in swine populations around the world (Brown, 2000). The infection is mainly related to acute respiratory symptoms which are frequently accompanied by bacterial co‐infections and may terminally result in or increased mortality among younger piglets, reduced weight gain in fatteners or abortion in carrying sows. Thus economic losses for the owner can be considerably high (Rajao et al., 2014; Vincent et al., 2014; Vincent et al., 2014).

Porcine influenza A viruses are members of the family of Orthomyxoviridae; they are single-stranded RNA viruses and consist of eight genome segments. Subtypes are designated according to the genetic and antigenic characteristics of the surface glycoproteins hemagglutinin (HA) and the neuraminidase (NA) (Cheung et al., 2007).

Glycan moieties with terminal sialic acids are acting as receptors for IAV attachment at the cell surface in the respiratory tract. Due to the expression of the receptors with α-2-6 or α-2-3-linked terminal sialic acids in in the porcine upper respiratory tract, swine are susceptible to IAVs of both avian and human origin (Byrd-Leotis et al., 2014; Trebbien et al., 2011; Walther et al., 2013). Therefore co-infections of porcine cells with avian and/or human IAV open possibilities for reassortment events (exchange of genome segments) between these viruses (Hass et al., 2011; Ma et al., 2009; Van Poucke et al., 2010; Zell et al., 2013). Such reassortants may display unexpected and difficult-to-predict phenotypic changes affecting, e.g. host and tissue tropism, virulence and antigenic make-up, in comparison to their parental viruses.

Figure 1. History and origin of porcine influenza A viruses (IAV) currently in circulation in Europe. It
should be noted that none of these porcine IAV rooted in swine populations.
Figure 1. History and origin of porcine influenza A viruses (IAV) currently in circulation in Europe. It should be noted that none of these porcine IAV rooted in swine populations.

Figure 1 gives an overview of the origin and reassortment history of porcine IAV which currently circulate in swine populations in Europe. Until 2009, three subtypes of IAV, H1N1, H1N2 and H3N2, were circulating in swine in Europe. The oldest of these lineages, H1N1, was introduced to the swine population in the late 1970s from an avian source and replaced the “classical” human 1918-derived H1N1 lineage which was in circulation in earlier years. As an influenza virus of avian origin the post 1970s H1N1 lineage is referred to as “avian-like” (av) H1N1 (Brown, 2013; Simon et al., 2014). In 1984,a human seasonal H3N2 virus reassorted with the H1avN1av subtype and a reassortant emerged that kept all six internal segments of avian origin and carried the HA (H3) and NA (N2) of the human virus (Kong et al., 2015). This reassortant established endemic status in swine populations in several but apparently not all European countries since then. A further reassortment, in 1994, affected the porcine H3N2 virus which exchanged its HA gene segment with that of another human seasonal H1N1 IAV to generate the porcine H1N2 lineage. This H1 subtype is referred to as “human-like” (hu) H1N2 (Brown, 1998). These lineages circulated at relative stability in European countries with some geographically restrictions regarding their prevalence (Brown, 2013; Kuntz-Simon et al., 2009). Viruses of the H1N1av lineage appeared to be responsible for the majority of infections in swine in Europe (Brown, 2000).

In 2009, a fourth player entered the field: the human pandemic H1N1 2009 influenza A virus (H1N1pdm). This virus itself is of multi-reassortant origin carrying segments of American avian (PB2, PA), human (PB1), classical swine (HA, NP, NS), and European swine (NA, NP) descendance(Neumann et al., 2009). In reference to the at least partial swine origin of this last human pandemic IAV, the infection in humans had been dubbed “swine flu”. Pigs seemed to be highly susceptible to this kind of IAV and transmission in a reverse zoonotic fashion from infected humans to swine was recorded at many locations worldwide. Since then H1N1pdm is spreading in the swine populations and cycles independently of human infections(Brookes et al., 2010).

In the wake of this so-called “swine flu” a European surveillance program for porcine influenza has been carried out in the years 2013-2015, the ESNIP3 project (Watson et al., 2015). Results showed that H1N1pdm is present in several European countries, and at particularlyhigh prevalence in Britain and Ireland. Presence of H1N1pdm of human origin in swine populations in Europe obviously disturbed the meticulous balance of the three authentically European porcine influenza virus lineage and lead to increased reassortment events. Among the reassortants affecting H and or N segments an H1pdmN2 lineage emerged in Germany which is in circulation, at low prevalence, now for several years (Starick et al., 2012; Watson et al., 2015). The HA protein of these reassortants has undergone significant changes and is antigenically distinguishable from bona fide H1pdm of human origin (Harder et al., 2013). Other reassortants (H1huN1av, H1dpmN1av, H3N1pdm) have been described but were obviously not able to sustain circulation (Watson et al., 2015). Furthermore, reassortants that have exchanged all or part of the six internal genome segments with H1N1pdm viruses were reported (Kong et al., 2015; Watson et al., 2015). In the U.S., porcine H3N2 or H1N1 viruses carrying the M gene segment of H1N1pdm were associated with enhanced swine-to-human transmission at agricultural fairs (Schicker et al. 2016). Such “variant” viruses were also sporadically reported from Europe but were not related to human infections. The prevalence of H1N1pdm among swine populations in Europe varies considerably (Figure 2). In contrast to the situation on the British Islands, the porcine subtype H1N1av still claims the highest prevalence on the European continent while subtypes H3N2 and H1huN2 were found at lower prevalence (Figure 2). Subtype H3N2 has not been detected in Denmark, Poland or the United Kingdom, and only one very few sporadic outbreaks have been reported from France (Watson et al. 2015).

Figure 2. Geographical restriction of HA subtypes of porcine influenza viruses currently in circulation Europe. Data are based on (reference) and own passive monitoring studies that commenced in 2015.
Figure 2. Geographical restriction of HA subtypes of porcine influenza viruses currently in circulation Europe. Data are based on (reference) and own passive monitoring studies that commenced in 2015.

Passive monitoring studies in several central and western European countries commenced after the termination of the ESNIP3 project in 2015 and are based at our laboratory. Preliminary data that accumulated during the first year of surveillance revealed an increasing prevalence of H1N1pdm and its reassortants. In addition, enhanced co-infection frequency and reassortment activity between the three co-circulating porcineEuropean H1 lineages was evident. It is not quite clear inasmuch these findings are skewed by the implementation of refined diagnostic tools developed by our laboratory: Detection of porcine IAV and characterization of HA (H1av, H1hu, H1pdm, H3) and NA (N1av, N1pdm, N2) subtypes and lineages is achieved by a set of three real time RT-qPCRs. Increased sensitivity of these assays allow the direct analysis of field samples (in particular of nasal swabs) independently of virus isolation in cell cultures (Henritzi et al. 2016). These studies will continue at least until end of 2017.

Continued surveillance of swine populations in Europe is essential to follow the evolution of porcine IAV. PorcineIAV can play an important role in the generation of new human pandemic viruses as demonstrated by the emergence of the 2009 H1N1 virus. Gaining insights into the dynamic changes in genotypes and the emergence of new phenotypes with potentially enhanced zoonotic propensities of porcine IAV is at the core of the OneHealth policy.



Recent studies on porcine IAV in the authors’ laboratory have been funded by a grant from IDT, Dessau, Germany. The authors are grateful to Aline Maksimov and CarlSell for excellent technical assistence.

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